The bone 2 cartilage 2 bone transition from sturgeons 2 sharks 2 bony fish

Short summary for those in hurry:
There is support in Pehrson 1940 for the origin of facial (dermal) bones on a cartilaginous template (contra Hall 2005) in a proximal shark descendant.

  1. Sturgeons (shark ancestors in the LRT) have facial bones sheathed to a cartilage template.
  2. Sharks lose all trace of bone, but keep the cartilage.
  3. Bony fish (shark descendants in the LRT) reacquire facial bones on a cartilage template

Backstory
Several recent reader comments disputed and/or cast doubt on the identity of shark skull bones (Fig. 2) and the shark-to-bony fish transition recovered by the large reptile tree (LRT, 1771+ taxa, see Fig. 1 diagram). Objections were  based on developmental grounds. One reader (CB) wrote: Most of the bones you’re trying to identify on shark chondrocrania are dermal bones. That means they don’t pre-form in cartilage. Which means animals without a bony skull cannot have them.”

That is the traditional view found in current textbooks.

First:
my guess is this comment resulted after reading any of several authors all citing Hall 2005, who wrote, “The vertebrate dermal skeleton includes the plate-like bones of the skull, and, in reptiles and fishes, also includes various scales, scutes, denticles and fin rays. Dermal bone forms via a process known as intramembranous ossification, with mesenchymal condensations differentiating directly into bone without a cartilaginous template.”

Second:
As everyone knows, no part of shark skulls is bone. It’s all cartilage. Nevertheless and despite obliteration and/or fusion of most skull sutures, shark ‘nasal’ templates still cover the snout and nares. Shark ‘frontal’ templates are still located between the eyes. I have retained tetrapod skull nomenclature for shark skull template elements in order to include shark taxa in the LRT.

Third:
A valid phylogenetic context, like the LRT (diagram in Figs 1, 4), is vital in matters like this. Taxon exclusion leading to an improper cladogram is the root cause of most prior misunderstandings, as readers well know.

Wagner and Aspenberg 2011 wrote:
“Bone is specific to vertebrates, and originated as mineralization around the basal membrane of the throat or skin, giving rise to tooth-like structures and protective shields in animals with a soft cartilage-like endoskeleton.”

That’s not correct. In sharks dentine and enamel from the skin and teeth are not bone. Instead, bone first appears in sturgeons and kin. Then it disappears in sharks only to reappear in bony fish + tetrapods, according to the LRT. Traditionally and mistakenly sturgeons were considered relatives of derived bony fish, which is part of the problem.

In sturgeons and paddlefish, Bemis et al. 1997 report, 
“the bones more or less closely ensheath the underlying endochondral rostrum”. Sharks lack this sheath of bone on the rostrum. Instead, remaining more flexible cartilage supports the skull and skeleton.

Figure 2. Acipenser brevirostrum, 1m typical length. Records up to 1.47m.

Figure 2. Acipenser brevirostrum, 1m typical length. Records up to 1.47m.

Keys to understanding this issue include:

  1. Elements of the dermocranium in shark outgroup taxa: sturgeons (Fig. 1) and paddlefish = bone sheath over cartilage.
  2. Elements of the dermocranium in sharks (Fig. 2) = prismatic cartilage
  3. Elements of the dermocranium in proximal shark descendants: the bowfin, Amia (Figs. 2, 3) = bone patches develop around sensory cells over a cartilage template, according to Pehrson 1940.
Figure 2. Fish evolution from Hybodus to Amia documenting the shark to bony fish transition.

Figure 2. Fish evolution from Hybodus to Amia documenting the shark to bony fish transition.

Pehrson 1940 examined
a series of embryonic stages of the extant bowfin, Amia calva (Fig. 3), one of the most primitive bony fish in the LRT. Pehrson 1940 reports: “Three different stages of the formation of the premaxillary are shown. The anterior, dental part of the bone is clearly distinguishable from the posterior and dorsal part, situated above the cartilage.”

The ontogenetic origin of bone in Amia (Fig. 3) first appears in embryos as tiny islands on the skull surface over a cartilage or pre-cartilage template. This proximal descendant of hybodontid sharks (Fig. 2) documents many skull homologies.

Figure x. Embryo development in the bowfin, Amia. The facial bones develop as buds surrounding dermal sensory organs 'floating' on top of a cartilage base.

Figure 3. Embryo development in the bowfin, Amia. The facial bones develop as buds surrounding dermal sensory organs ‘floating’ on top of a cartilage (chondral) and prechondral base.

It is noteworthy
that the appearance of bone surrounding sensory cells all over the skull in bony fish followed the reduction of the long, sensory-cell-filled rostrum in bony fish. Taking the other evolutionary route, other shark descendants (e.g. hammerheads, skates, rays, goblin sharks, elephant-nosed chimaera, sawfish), further elongated the rostrum for increased acuity in finding bottom-dwelling prey.

Pehrson also described
the appearance of ossification where prior cartilage dissolved, convergent with the process of fossilization. Thereafter some embryos began to develop ossified skull bones without a cartilaginous template, in accord with Hall 2005, who did not cite Pehrson 1940.

Surprisingly,
Pehrson was keen on naming fish bones in accord with those of pre-tetrapods. He reports, “There seems to be no doubt that the intertemporal and supratemporal parts of the developing composite bone correspond to the similarly named bones in Osteolepidae and Rhizodontidae.” Not sure if Pehrson was the first to do this, but it should be standard.

Supporting evidence that sturgeons are shark ancestors:
According to Wikipedia, notable characteristics of Acipenseriformes include:

  1. Cartilaginous endoskeleton – as in sharks and fish more primitive than sharks
  2. Lack of vertebral centrum – as in fish more primitive than sharks
  3. Spiral valve intestine – as in sharks, bichirs, gars and lungfish, the last two by reversals.
  4. Conus arteriosus = infundibulum, a conical pouch found in the heart from which the pulmonary trunk artery arises (not sure how this relates, but there it is).

Bemis et al. report,
“Acipenseriforms are central to historical ideas about the classification and evolution of fishes.”

Indeed. The LRT comes to the same conclusion.

“Acipenseriforms also are noteworthy because of their unusual mixture of characters, which caused early debate about their classification. Two aspects of living Acipenseriformes were especially problematic for early ichthyologists: (1) reduced ossification of the endoskeleton combined with presence of an extensive dermal skeleton; and (2) the presence of a hyostylic jaw suspension and protrusible palatoquadrate recalling the jaws of sharks.”

These aspects are not problematic of sturgeons and paddlefish are basal to sharks.

The palatoquadrate is neither a palatine nor a quadrate. It is largely homologous to the lacrimal with fusion of the tiny quadrate and tall, curved, preopercular in most taxa, fusion of the premaxilla and maxilla (tooth-bearing elements) on taxa with teeth. The former and future jugal is also typically fused.

Figure 5. Sturgeon mouth animated from images in Bemis et al. 1997. This similar to ostracoderms, basal to sharks.

Figure 5. Sturgeon mouth animated from images in Bemis et al. 1997. This similar to ostracoderms, basal to sharks.

“The current conventional view (developed and refined by many authors… holds that Acipenseriformes evolved from a ‘paleonisciform’ ancestor via paedomorphic reduction of the skeleton and specialization of the feeding system, but there is much more to the history of ideas about the systematics of this group.”

That is incorrect according to the LRT, which tests a wider gamut of fish and nests traditional acipenseriformes basal to unarmored sharks and derived from armored osteostracoderms (Fig. 4). There was no paedomorphic reduction of the skeleton at the origin of sturgeons. The sturgeon feeding system is not ‘specialized’. It is primitive.


References
Bemis WE, Findeis EK and Grande L 1997. An overview of Acipenseriformes. Environmental Biology of Fishes 48: 25–71, 1997.
Gillis JA 2019. ‘Secondary’ cartilage and the vertebrate dermal skeleton in Reference Module in Life Sciences.
Hall BK 2005. Bones and Cartilage. Academic Press, London. ISBN: 978-0-12-319060-4
Maisey JG 1983. Cranial anatomy of Hybodus basanus Egerton from the Lower Cretaceous of England. American Museum Novitates 2758:1–64.
Maisey JG 1987. Cranial Anatomy of the Lower Jurassic Shark Hybodus reticulatus
(Chondrichthyes: Elasmobranchii), with Comments on Hybodontid Systematics. American Museum Novitates 2878: 1–39.
Pehrson GT 1940. The development of dermal bones in the skull of Amia calva. Acta Zoologica 21:1–50.
Wagner DO and Aspenberg P 2011. Where did bone come from? An overview of its evolution. Acta Orthopaedica. 82(4):393–398.
The Skull, Volume 1. Eds. Hanken J and Hall BK University of Chicago Press Books, 1993.

https://en.wikipedia.org/wiki/Acipenseriformes
https://www.zoology.ubc.ca/~millen/vertebrate/Bio204_Labs/Lab_3__Skull.html
G Torsten Pehrson bio

12 thoughts on “The bone 2 cartilage 2 bone transition from sturgeons 2 sharks 2 bony fish

  1. OK – where to begin…

    1. Your guess that this comes from reading Hanken 2005, or something citing it, is unlikely to be accurate given that I learned all about it as an undergraduate in the 1980’s. I also saw it for myself in graduate school in the 1990’s, when I did some clearing and staining of alligator embryos.

    2. Your claim that shark denticles (dentin and enamel) are not bone is incorrect. The earliest known bone is exoskeletal and has these very components. The only differences between enamel, dentine, and what the average person would call bone are the proportions of hydroxyapatite and protein components and the orientation of hydroxyapatite crystals. That’s it. Enamel has very little organic material, which is why it’s so hard, but the mineral fraction is indistinguishable from what one sees in other osseous tissue.

    If you think shark denticles are not homologous with a structure in some other vertebrate, fine – but that doesn’t somehow change their developmental origin (which is actually more complex than for dermal bone) or underlying histology.

    3. There is no such thing as a “template” for a dermal bone on the chondrocranium. Dermal bones may form over cartilage, but since they’re not forming within it, there won’t be any sort of biologically meaningful ‘template” in the underlying cartilage. Full stop.

    Airports are usually build on flat, level ground. That does not mean that some aspect of the runway could be found in the soil before construction began.

    I would have described your assessments as “apples and oranges,” but apples and oranges are, at a deep level, homologous. A better comparison is between oranges and orange-colored golf balls.

    Likewise, there are neither obliterated nor fused “sutures” in a chondrocranium for the very simple reason that a suture, by definition, is a joint formed between two or more bones separated by fibrous tissue. There are no sutures in cartilage. The early chondrocranium is comprised of many parts that eventually merge, but not with sutures. (The parts of the chondrocranium that ossify may show sutures, but these are between the bones – not the preceding cartilage.)

    The term “suture” is sometimes applied to other types of bony contacts. Some would argue that true sutures only occur in the skull, though the contacts between the centrum and neural arch of a vertebra are arguably of the same type as those in the dermatocranium. But in all cases, the sutures are between bones and only bones.

    If you want to convince people otherwise, mapping things out on a tree won’t work. You’ll have to find the direct biological connection between what you claim is a chondrocranial template and the dermal bone that might form in the same area. That means actually doing the experimental evo-devo. Which people have been doing for decades, all without seeing anything like you claim.

    4. Again, pointing to your cladograms in support of your claim is a waste of time. I am ignoring your trees for the sake of this argument and will continue to do so.

    You include your interpretations in the matrix, thus rendering such arguments circular to begin with. Indeed, that appears to be part of your rationale for making these hology assessments in the first place – you want more characters. Even though it’s like finding the homologue for my eyelids in the feeding apparatus of a sea urchin.

    Moreover, the distinctions seen by generations of developmental biologists were known long before the advent of modern phylogenetics – if something doesn’t have a cartilaginous precursor during development, its position on a phylogeny will be irrelevant.

    5. I have no idea why the presence of dermal bone where cartilge used to be is relevant. there may be structural constraints that would render the presence of both bone and cartilage incompatible,

    6. I read through Pehrson and found nothing that would support any sort of radical departure from modern interpretations. In any event, it was published 80 years ago. Grande and Bemis’ SVP memoir on amiid morphology – which includes extensive developmental data – would be a better source of information.

    At this point, I don’t know who’s wasting more time – you by trying to defend fundamentally indefensible interpretations, or me by trying to explain this indefensibility to you. Hopefully, at least some of your readers will listen to me.

    • Chris, Thank you for your reply.
      1. re: Hanken 2005, Hall 2005
      You gave no other citation, nor referenced your undergraduate experience. Hanken 2005 provides something for readers to look up for themselves.

      2. (dentin and enamel) are not bone is incorrect.
      Dentin and enamel are distinct from bone. That’s why they have different names from each other and from bone.

      3. There is no such thing as a “template”
      That’s the word in the quote from Hall 2005.

      4. Dermal bones may form over cartilage,
      Exactly. Thank you.

      5. There are no sutures in cartilage. The early chondrocranium is comprised of many parts that eventually merge, but not with sutures.
      That’s interesting. Please provide citations. Ontogeny recapitulates phylogeny. In any case, the phylogeny indicates the loss of bone followed generations later by the reappearance of bone. Neotony. Reversal. I’m reporting results. The mechanism is for others to report.

      6. pointing to your cladograms in support of your claim
      I am reporting results. Not making claims. It is up to others to repeat the methods to verify or invalidate the results. Until then the results sit out there in limbo.

      7. like finding the homologue for my eyelids in the feeding apparatus of a sea urchin.
      Stop being silly, Chris. Others have seen similar arguments proposed by Creationists. Stay grounded.

      8. if something doesn’t have a cartilaginous precursor
      Take another look. There’s a logic misstep here. Sharks have jaws that anchor teeth. So do bowfins. Seems we have a cartiaginous precursor here.

      9. I have no idea why the presence of dermal bone where cartilge (sic) used to be is relevant.
      I’m not as interested in ‘why’ questions. I am interested in ‘what’ questions at present. Traditional paleontology has open wounds wherever sister taxa do not closely resemble one another.

      10. I read through Pehrson and found nothing that would support any sort of radical departure
      If Pehrson is not radically different from current interpretations, then there is no reason to disrespect it on account of age. Even so, thank you for the Grande and Bemis citation, which is new to me.

      11. I don’t know who’s wasting more time.
      Please provide a citation that includes sharks, sturgeons, paddlefish and bony fish that tests ‘apples to apples’ and includes skull element characters. We need a prior study to provide a competing hypothesis to the LRT. To simply say I have “fundamentally indefensible interpretations” without providing a better interpretation that uses the same nomenclature across all the above taxa is not going to work this time. As everyone knows, all vertebrates are somehow related. We need to start talking about them using one common standard nomenclature and stop hiding behind different names for fish and reptile skull bones and shark cartilage topography.

      • My sea urchin comment may have been silly, but it’s also an example of the very same kind of mistakes you’re making. A sea urchin’s jaw apparatus opens and closes, kind of like a five-way eyelid, but they’re not homologous.

        An example I use with my beginning students might be a better analogy. Ancestrally, tetrapods have some sort of bone in the chest area. In mammals, it’s the sternum. This is true also for birds. Crocodylians and (most) squamates have a bone in the same area, but it’s not a sternum – it’s an interclavicle. They have a sternum, but it remains unossified (though it may calcify in very old individuals – these would be deposits of calcium carbonate, not bone). The bony sternum ossifies within its cartilaginous precursor, and the interclavicle is dermal. Moreover, sterna can connect directly to parts of the axial skeleton (e.g. dorsal ribs), but the interclavicle does not. No homology there at all. A few animals actually have both (e.g. monotremes). What you’re doing is, quite literally, the very same as coding interclavicle characters for a placental.

        My other comments (e.g. that sutures are a specific type of joint) are based on what amounts to common vertebrate morphology knowledge; a standard vertebrate anatomy textbook will probably tell you about it, though human anatomy texts probably go into more depth.

        (And yes, dentine and enamel are basically types of bone. That they’re called something else doesn’t matter; the veery and european blackbird are both kinds of thrush, even though the word “thrush” isn’t in their name. Of course denine and enamel are different from what one might colloquially call bone, but there are major differences between, for example, cancellous and cortical bone. All of these mineralized tissues are variants of the same thing.)

        “The mechanism is for others to find out.” The problem is that you’re not identifying something requiring some sort of “mechanism.” We know how chondrocrania develop. We know how parts of it ossify. We also know how the dermatocranium forms. We know how these happen based on gross morphology, histology, and developmental genetics. This information is enough to falsify the hypothesis that one can find a developmental correspondence between the nasal and the central part of the dorsal roof of a chondrocranium. It just isn’t there – hence my decision to ignore your trees, as they have no bearing on the question.

        If you want to claim that dermatocrania were lost and then regained, you’d be better off looking at homeotic changes that reactivate genes. Bipes, for example, is not the basalmost amphisbaenian, but it, unlike any other amphisbaenian, has fully formed hindlimbs. At some point in amphisbaenian phylogeny, one or more regulatory genes turned off the genes that encoded for forelimb development, and in the lineage giving rise to Bipes, they turned on again. There is no precursor or homologue for the forelimb in any limbless amphisbaenian.

        I’m not saying this is what happened – not because it would be speculative, but because I don’t buy your tree. But it would at least free you from the pointless search for homologues that just aren’t there. At the very least, you should correct your codings to reflect the absence of om

        Also – I wasn’t “bashing” Pehrson because of its age. The fields of embryology, comparative morphology, and development have advanced quite a bit since 1940, and one would think a more recent reference would account for some of these advancements.

        I really am sorry I can’t help you – but as long as you insist there are homologues of some sort within a shark chondrocranium for a dermal bone, I can’t.

      • Chris, let’s keep to the subject and avoid convergence and analogs (birds, Bipes, etc.). You wrote: “We know how chondrocrania develop.” Do you know how chondrocrania develop in Hybodus and Amia, transitional taxa from sharks to bony fish? That’s all that matters, because after that transition, anything can happen. Do you know how chondrocrania disappear from sturgeons and paddlefish to sharks? Again, that’s all that matters. This latest blogpost gathered more data pertinent to the present subject: https://pterosaurheresies.wordpress.com/2020/12/08/why-sharks-have-no-bones-borrell-2014/

  2. Also – the fact that a shark’s Meckel’s cartilage and palatoquadrate bear teeth means nothing, really. Lots of bones independently develop teeth. Most fish have teeth on almost every bone involved in the oral cavity. They’re on the branchial arches, too – at least in some forms. A tooth results from an inductive relationship between early-developing tissues unrelated to the internal skeleton, so whether they’re on a cartilaginous element of one fish and on a dermal bone in another doesn’t really tell us anything.

      • No. That would be the equivalent of being asked to add 2 and 2. It’s very basic knowledge that a successful PhD candidate can be assumed to know.

        That’s not intended to be snark. It’s a statement of fact. If a student studying vertebrate morphology doesn’t know the basic developmental history of the skull, he or she won’t get to the defense stage. Basic homology assessment is one of the first things one learns.

        There’s an old saying that thinking outside the box is OK, but only if you remember where the box is. The box is there for a reason, and it has nothing to do with protecting the reputations of older scholars.

        Someone defending a genetics thesis is unlikely to be asked to discuss the basic structure of DNA, or to complete some Punnett squares of the type you see in introductory biology classes, for the very same reason. A genetics student lacking these skills wouldn’t be able to complete the research for a thesis, much less defend it.

      • So, how are we leaving this situation? Crossopterygians get tetrapod skull nomenclature? Lungfish less so? Paleoniscoids less so? Osteichthyes less so? (ref: Fish Skulls by Gregory 1933) Sharks: don’t even try. That’s not good. I’d like to find a universal common language if possible.

  3. “I’d like to find a universal common language if possible.”

    That’s the whole point I’m trying to make. When it comes to the dermal bones of a skull, there’s no common language to be found in the chondrocranium of the shark. There’s no common language between a shark’s chondrocranium and my liver, either. There’s no direct developmental or genetic connection.

    Notice how we don’t use terms intended to describe parts of the wrist on isolated caudal vertebrae? Or terms describing parts of the interclavicle on the sternum? This is basically what you’re trying to do.

    I’m really, truly not trying to be a jerk here. If you’re looking for some sort of homology between the frontal of a bowfin and the tegmen of a nurse shark braincase, you’re wasting your time. (I appear to be wasting mine by trying to explain this to you.) There won’t be any homology.

    I understand you want to find new characters for your phylogenetic work. Fair enough. But you’re only misleading yourself if your search for characters prompts false homology assessments.

    I really want to you think about your approach. Are you recognizing potential homology, or are you looking for it? They’re not the same thing, and one is more likely to lead down the path of self-delusion.

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